Meiotic self-pairing of the Psalidodon (Characiformes, Characidae) iso-B chromosome: A successful perpetuation mechanism

Abstract

B chromosomes are non-essential additional genomic elements present in several animal and plant species. In fishes, species of the genus Psalidodon (Characiformes, Characidae) harbor great karyotype diversity, and multiple populations carry different types of non-essential B chromosomes. This study analyzed how the dispensable supernumerary B chromosome of Psalidodon paranae behaves during meiosis to overcome checkpoints and express its own meiosis-specific genes. We visualized the synaptonemal complexes of P. paranae individuals with zero, one, or two B chromosomes using immunodetection with anti-medaka SYCP3 antibody and fluorescence in situ hybridization with a (CA) 15 microsatellite probe. Our results showed that B chromosomes self-pair in cells containing only one B chromosome. In cells with two identical B chromosomes, these elements remain as separate synaptonemal complexes or close self-paired elements in the nucleus territory. Overall, we reveal that B chromosomes can escape meiotic silencing of unsynapsed chromatin through a self-pairing process, allowing expression of their own genes to facilitate regular meiosis resulting in fertile individuals. This behavior, also seen in other congeneric species, might be related to their maintenance throughout the evolutionary history of Psalidodon .

B Chromosomes in Psalidodon scabripinnis (Characiformes, Characidae) Species Complex

“…Furthermore, in an extensive analysis based on satellite DNA mining by NGS and bioinformatics, Silva et al [ 46 ] revealed the presence of 14 families of satDNA clustered in BM and distributed symmetrically. All repetitive DNA mapped in this B chromosome suggested that the B chromosome of P. paranae is also an isochromosome, which was later confirmed by meiotic studies showing their self-pairing [ 39 ], as revealed in the B chromosome of P. scabripinnis [ 38 ]. The higher content of repetitive DNAs in this B chromosome than in standard chromosomes constitutes the different heterochromatin patterns between them [ 45 ], indicating that B chromosomes follow their own evolutionary pathway.…”

“…Recent studies performed on Psalidodon indicated differential gene expression in individuals carrying B chromosomes [ 21 , 39 , 40 , 74 ]. A transcriptome analysis showed a high expression of two paralog genes on the B chromosome related to the cell cycle ( nobox and msh4 ) in females [ 21 ].…”

“…The large metacentric B chromosome variants of P. scabripinnis and P. paranae are isochromosomes that self-pair during meiosis [ 8 , 38 , 39 ]. Furthermore, when meiotic cells of P. paranae have two iso-B chromosomes, they self-pair and optionally pair with each other [ 39 ].…”

“…The large metacentric B chromosome variants of P. scabripinnis and P. paranae are isochromosomes that self-pair during meiosis [ 8 , 38 , 39 ]. Furthermore, when meiotic cells of P. paranae have two iso-B chromosomes, they self-pair and optionally pair with each other [ 39 ]. This ability may confer an adaptive advantage to these elements to cross-checkpoints during the cell cycle and succeed through divisions.…”

“…Numbers in square brackets refer to references. On the right, features involving the B chromosomes that still need further investigation [ 8 , 21 , 38 , 39 , 40 , 41 ].…”